Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Abstract

Tremor imposes an important limit to the accuracy of fine movements in healthy individuals and can be a disabling feature of neurological disease. Voluntary slow finger movements are not smooth but are characterized by large discontinuities (i.e., steps) in the tremor frequency range (approximately 10 Hz). Previous studies have shown that these discontinuities are coherent with activity in the primary motor cortex (M1), but that other brain areas are probably also involved. We investigated the contribution of three important subcortical areas in two macaque monkeys trained to perform slow finger movements. Local field potential and single-unit activity were recorded from the deep cerebellar nuclei (DCN), medial pontomedullary reticular formation, and the intermediate zone of the spinal cord (SC). Coherence between LFP and acceleration was significant at 6 to 13 Hz for all areas, confirming the highly distributed nature of the central network responsible for this activity. The coherence phase at 6 to 13 Hz for DCN and pontomedullary reticular formation was similar to our previous results in M1. By contrast, for SC the phase differed from M1 by approximately pi rad. Examination of single-unit discharge confirmed that this was a genuine difference in neural spiking and could not be explained by different properties of the local field potential. Convergence of antiphase oscillations from the SC with cortical and subcortical descending inputs will lead to cancellation of approximately 10 Hz oscillations at the motoneuronal level. This could appreciably limit drive to muscle at this frequency, thereby reducing tremor and improving movement precision.

Fig. 1.

(A and B) Raw data showing discontinuities during slow finger movements in monkeys. Examples of raw data during a single trial of the behavioral task. Actual finger displacement (black) is shown against the allowed target window (gray). Finger acceleration is shown, as is LFP from M1, PMRF, DCN, and SC, respectively. (C) Acceleration power during flexion ramp phase of the task. (D) LFP power during flexion ramp from the four different brain areas. (E–L) Coherence between LFP and finger acceleration, averaged over all LFPs and all sessions for different areas of the brain and SC. Coherence was calculated during flexion (E–H) or extension (I–L) tracking movements. Dashed line shows the significance level (P < 0.05). Shaded area shows the 6- to 13-Hz tremor band used for subsequent analysis.

Fig. 2.

Circular mean coherence phase calculated from individual LFP-acceleration phase spectra, averaged over both monkeys during flexion (A–C) and extension (D–F) movements. Average phase (mean ± SEM) was calculated for DCN (green, n = 331), PMRF (blue, n = 179), and SC (red, n = 52) and compared with average M1 phase (black, n = 474). Shaded area shows the 6 to 13 Hz range. (G and H) rose plots of the circular mean phase of each LFP from 6 to 13 Hz during flexion (G) and extension (H). Arrows and bars show mean and 95% confidence limits for all of the recordings within that area. The bin width in rose plots is π/24.

Fig. 3.

(A) Average coherence between cell spiking and acceleration, for cells from M1 and SC. Dashed lines show significance limits (P < 0.05) for each plot. (B) Circular mean coherence phase between cell spiking and acceleration. (C) Rose plots of the phase for each cell averaged over the 6- to 13-Hz range. (D and E) Spike-triggered average of rectified EMG from the flexor digitorum profundus (D) and first dorsal interosseus (E) muscles, triggered by discharge of SC cells. (F–H) Same as A–C, but red traces relate to the subset of premotor SC cells, which showed postspike facilitation in spike-triggered averages of EMG.

Fig. 4.

Schematic diagrams of possible neural circuits to reduce oscillations in motoneuron firing: (A) frequency selective attenuation (notch filter); (B) recurrent inhibition; (C), frequency selective phase inversion; (D) sensory feedback from periphery. MN, motoneuron; IN, interneuron. E is an example of temporal shaping with excitatory input to membrane potential of motoneuron. Dashed line is the threshold.